The ventral striatum dissociates information expectation, reward anticipation, and reward receipt

Do dopaminergic reward structures represent the expected utility of information similarly to a reward? Optimal experimental design models from Bayesian decision theory and statistics have proposed a theoretical framework for quantifying the expected value of information that might result from a query. In particular, this formulation quantifies the value of information before the answer to that query is known, in situations where payoffs are unknown and the goal is purely epistemic: That is, to increase knowledge about the state of the world. Whether and how such a theoretical quantity is represented in the brain is unknown. Here we use an event-related functional MRI (fMRI) task design to disentangle information expectation, information revelation and categorization outcome anticipation, and response-contingent reward processing in a visual probabilistic categorization task. We identify a neural signature corresponding to the expectation of information, involving the left lateral ventral striatum. Moreover, we show a temporal dissociation in the activation of different reward-related regions, including the nucleus accumbens, medial prefrontal cortex, and orbitofrontal cortex, during information expectation versus reward-related processing.

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A probabilistic atlas of the human ventral tegmental area (VTA) based on 7 Tesla MRI data

Brain Structure and Function ◽

10.1007/s00429-021-02231-w ◽

2021 ◽

Vol 226 (4) ◽

pp. 1155-1167 ◽

Cited By ~ 1

Author(s):

Anne C. Trutti ◽

Laura Fontanesi ◽

Martijn J. Mulder ◽

Pierre-Louis Bazin ◽

Bernhard Hommel ◽

...

Keyword(s):

Ventral Tegmental Area ◽

Region Of Interest ◽

Reward Processing ◽

7 Tesla ◽

Subcortical Structures ◽

7 Tesla Mri ◽

Subcortical Nuclei ◽

Ventral Tegmental ◽

The Brain

AbstractFunctional magnetic resonance imaging (fMRI) BOLD signal is commonly localized by using neuroanatomical atlases, which can also serve for region of interest analyses. Yet, the available MRI atlases have serious limitations when it comes to imaging subcortical structures: only 7% of the 455 subcortical nuclei are captured by current atlases. This highlights the general difficulty in mapping smaller nuclei deep in the brain, which can be addressed using ultra-high field 7 Tesla (T) MRI. The ventral tegmental area (VTA) is a subcortical structure that plays a pivotal role in reward processing, learning and memory. Despite the significant interest in this nucleus in cognitive neuroscience, there are currently no available, anatomically precise VTA atlases derived from 7 T MRI data that cover the full region of the VTA. Here, we first provide a protocol for multimodal VTA imaging and delineation. We then provide a data description of a probabilistic VTA atlas based on in vivo 7 T MRI data.

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Addiction as a brain disease revised: why it still matters, and the need for consilience

Neuropsychopharmacology ◽

10.1038/s41386-020-00950-y ◽

2021 ◽

Cited By ~ 1

Author(s):

Markus Heilig ◽

James MacKillop ◽

Diana Martinez ◽

Jürgen Rehm ◽

Lorenzo Leggio ◽

...

Keyword(s):

Spontaneous Remission ◽

Brain Disease ◽

Substance Addiction ◽

Alternative Reinforcement ◽

Sociocultural Perspectives ◽

Compulsive Behaviors ◽

Biological Substrate ◽

Neural Signature ◽

The Brain ◽

Neuroscience Community

AbstractThe view that substance addiction is a brain disease, although widely accepted in the neuroscience community, has become subject to acerbic criticism in recent years. These criticisms state that the brain disease view is deterministic, fails to account for heterogeneity in remission and recovery, places too much emphasis on a compulsive dimension of addiction, and that a specific neural signature of addiction has not been identified. We acknowledge that some of these criticisms have merit, but assert that the foundational premise that addiction has a neurobiological basis is fundamentally sound. We also emphasize that denying that addiction is a brain disease is a harmful standpoint since it contributes to reducing access to healthcare and treatment, the consequences of which are catastrophic. Here, we therefore address these criticisms, and in doing so provide a contemporary update of the brain disease view of addiction. We provide arguments to support this view, discuss why apparently spontaneous remission does not negate it, and how seemingly compulsive behaviors can co-exist with the sensitivity to alternative reinforcement in addiction. Most importantly, we argue that the brain is the biological substrate from which both addiction and the capacity for behavior change arise, arguing for an intensified neuroscientific study of recovery. More broadly, we propose that these disagreements reveal the need for multidisciplinary research that integrates neuroscientific, behavioral, clinical, and sociocultural perspectives.

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Setting priorities for research: a practical application of ‘payback’ and expected value of information

Health Economics ◽

10.1002/hec.1225 ◽

2007 ◽

Vol 16 (12) ◽

pp. 1345-1357 ◽

Cited By ~ 14

Author(s):

Rachael L. Fleurence

Keyword(s):

Value Of Information ◽

Expected Value ◽

Practical Application ◽

Expected Value Of Information

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Review for "Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum"

10.1002/brb3.1987/v2/review1 ◽

2020 ◽

Keyword(s):

Ventral Striatum ◽

Neural Correlates ◽

Reward Processing

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The effects of the form of sugar (solid vs. beverage) on body weight and fMRI activation: A randomized controlled pilot study

PLoS ONE ◽

10.1371/journal.pone.0251700 ◽

2021 ◽

Vol 16 (5) ◽

pp. e0251700

Author(s):

John W. Apolzan ◽

Owen T. Carmichael ◽

Krystal M. Kirby ◽

Sreekrishna R. Ramakrishnapillai ◽

Robbie A. Beyl ◽

...

Keyword(s):

Body Weight ◽

Energy Homeostasis ◽

Pilot Trial ◽

Brain Regions ◽

Reward Processing ◽

Daily Consumption ◽

Fed State ◽

Randomized Controlled ◽

The Right ◽

The Brain

Objective To test if sugar sweetened beverages (SSBs) and sugar sweetened solids (SSSs) have differential effects on body weight and reward processing in the brain. Methods In a single blind randomized controlled pilot trial (RCT), twenty participants with BMI between 20 and 40 kg/m2 were randomized to consume a 20 fluid ounce soda (SSB, 248 kcal) or the equivalent in solid form (SSS; similar to thick gelatin or gummy candy) daily. At baseline and day 28, fasting body weight and fed-state BOLD fMRI of the brain were assessed. Differences in fMRI signals between views of low-fat (LF (<30%)) high sugar (HS (>30%)) food, and non-food images were calculated in brain regions implicated in energy homeostasis, taste, and reward. Results All participants in the SSB (6F 4M; 8 Caucasian; 36±14 y, 28.2±5.5 kg/m2; Mean±SD) and SSS (3F 7M; 6 Caucasian; 39±12; 26.3±4.4) groups completed the study. Weight change was 0.27±0.78 kg between SSB and SSS participants. Changes in the fMRI response to LF/HS foods in reward, homeostatic and taste regions tended to not be different between the groups over the four weeks. However, activation of the right substantia nigra increased following the SSB but decreased activation following the SSS in response to LF/HS foods over 28 days (-0.32±0.12). Ratings of wanting for LF/HS foods were correlated with activation in several brain regions, including the OFC. Conclusions Change in weight was modest between the groups in this study. Daily consumption of a SSB over 28 days led to mixed responses to LF/HS foods in areas of the brain associated with reward. Ratings of wanting are correlated with fMRI activation inside an MRI scanner.

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Distinct Processing of Selection and Execution Errors in Neural Signatures of Outcome Monitoring

10.1101/853317 ◽

2019 ◽

Author(s):

Faisal Mushtaq ◽

Samuel D. McDougle ◽

Matt P. Craddock ◽

Darius E. Parvin ◽

Jack Brookes ◽

...

Keyword(s):

Behavioral Adjustment ◽

Behavioral Changes ◽

Behavioral Correlates ◽

Feedback Information ◽

Future Action ◽

Outcome Monitoring ◽

Frontal Negativity ◽

Neural Signature ◽

The Brain ◽

Insight Into

AbstractLosing a point playing tennis may result from poor shot selection or poor stroke execution. To explore how the brain responds to these different types of errors, we examined EEG signatures of feedback-related processing while participants performed a simple decision-making task. In Experiment 1, we used a task in which unrewarded outcomes were framed as selection errors, similar to how feedback information is treated in most studies. Consistent with previous work, EEG differences between rewarded and unrewarded trials in the medial frontal negativity (MFN) correlated with behavioral adjustment. In Experiment 2, the task was modified such that unrewarded outcomes could arise from either poor execution or selection. For selection errors, the results replicated that observed in Experiment 1. However, unrewarded outcomes attributed to poor execution produced larger amplitude MFN, alongside an attenuation in activity preceding this component and a subsequent enhanced error positivity (Pe) response in posterior sites. In terms of behavioral correlates, only the degree of the early attenuation and amplitude of the Pe correlated with behavioral adjustment following execution errors relative to reward; the amplitude of the MFN did not correlate with behavioral changes related to execution errors. These results indicate the existence of distinct neural correlates of selection and execution error processing and are consistent with the hypothesis that execution errors can modulate action selection evaluation. More generally, they provide insight into how the brain responds to different classes of error that determine future action.Significance StatementTo learn from mistakes, we must resolve whether decisions that fail to produce rewards are due to poorly selected action plans or badly executed movements. EEG data were obtained to identify and compare the physiological correlates of selection and execution errors, and how these are related to behavioral changes. A neural signature associated with reinforcement learning, a medial frontal negative (MFN) ERP deflection, correlated with behavioral adjustment after selection errors relative to reward outcomes, but not motor execution errors. In contrast, activity preceding and following the MFN response correlated with behavioral adjustment after execution errors relative to reward. These results provide novel insight into how the brain responds to different classes of error that determine future action.

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Reward-Associated Gamma Oscillations in Ventral Striatum Are Regionally Differentiated and Modulate Local Firing Activity

Journal of Neurophysiology ◽

10.1152/jn.00432.2009 ◽

2010 ◽

Vol 103 (3) ◽

pp. 1658-1672 ◽

Cited By ~ 50

Author(s):

Tobias Kalenscher ◽

Carien S. Lansink ◽

Jan V. Lankelma ◽

Cyriel M. A. Pennartz

Keyword(s):

Ventral Striatum ◽

Phase Locking ◽

Gamma Oscillations ◽

Brain Regions ◽

Reward Processing ◽

Temporal Organization ◽

Gamma Activity ◽

Neural Ensembles ◽

Gamma Range ◽

Gamma Power

Oscillations of local field potentials (LFPs) in the gamma range are found in many brain regions and are supposed to support the temporal organization of cognitive, perceptual, and motor functions. Even though gamma oscillations have also been observed in ventral striatum, one of the brain's most important structures for motivated behavior and reward processing, their specific function during ongoing behavior is unknown. Using a movable tetrode array, we recorded LFPs and activity of neural ensembles in the ventral striatum of rats performing a reward-collection task. Rats were running along a triangle track and in each round collected one of three different types of rewards. The gamma power of LFPs on subsets of tetrodes was modulated by reward-site visits, discriminated between reward types, between baitedness of reward locations and was different before versus after arrival at a reward site. Many single units in ventral striatum phase-locked their discharge pattern to the gamma oscillations of the LFPs. Phase-locking occurred more often in reward-related than in reward-unrelated neurons and LFPs. A substantial number of simultaneously recorded LFPs correlated poorly with each other in terms of gamma rhythmicity, indicating that the expression of gamma activity was heterogeneous and regionally differentiated. The orchestration of LFPs and single-unit activity by way of gamma rhythmicity sheds light on the functional architecture of the ventral striatum and the temporal coordination of ventral striatal activity for modulating downstream areas and regulating synaptic plasticity.

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